Osmoregulated Periplasmic Glucans Transmit External Signals Through Rcs Phosphorelay Pathway in Yersinia enterocolitica.

Beizhong Han,Dingyu Liu,Can Huang,Jingyu Chen,Jiao Meng,Xiaoning Huang

doi:10.3389/fmicb.2020.00122

Beizhong Han, Dingyu Liu + Show 4 more

Open Access

https://doi.org/10.3389/fmicb.2020.00122

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Abstract

Fast response to environmental changes plays a key role in the transmission and pathogenesis of Yersinia enterocolitica. Osmoregulated periplasmic glucans (OPGs) are known to be involved in environmental perception of several Enterobacteriaceae pathogens; however, the biological function of OPGs in Y. enterocolitica is still unclear. In this study, we investigated the role of OPGs in Y. enterocolitica by deleting the opgGH operon encoding enzymes responsible for OPGs biosynthesis. Complete loss of OPGs in the ΔopgGH mutant resulted in decreased motility, c-di-GMP production, biofilm formation and smaller cell size, whereas the overproduction of OPGs through restoration of opgGH expression promoted c-di-GMP/biofilm production and increased antibiotic resistance of Y. enterocolitica. Gene expression analysis revealed that opgGH deletion reduced transcription of flhDC, ftsAZ, hmsT and hmsHFRS genes regulated by the Rcs phosphorelay system, whereas additional deletion of rcs family genes (rcsF, rcsC, or rcsB) reversed this effect and restored motility and c-di-GMP/biofilm production but further reduced cell size. Furthermore, disruption of the Rcs phosphorelay increased the motility and promoted the induction of biofilm and c-di-GMP production regulated by OPGs through upregulating the expression of flhDC, hmsHFRS, and hmsT. However, deletion of genes encoding the EnvZ/OmpR phosphorelay downregulated the flhDC, hmsHFRS and hmsT expression, leading to the decreased motility and prevented the induction of biofilm and c-di-GMP production regulated by OPGs. These results indicated that Rcs phosphorelay had the effect on OPGs-mediated functional responses in Y. enterocolitica. Our findings disclose part of the biological role of OPGs and the underlying molecular mechanisms associated with Rcs system in the regulation of the pathogenic phenotype in Y. enterocolitica.

Highlights

Yersinia enterocolitica is a common foodborne pathogen which causes a zoonotic disease called yersiniosis manifested in humans by acute gastroenteritis and sometimes more serious conditions such as pseudoappendicitis and even sepsis (Huovinen et al, 2010; Bari et al, 2011; Fabrega and Vila, 2012)
It was found that regulator of capsule synthesis (Rcs) and EnvZ/OmpR phosphorelays had opposite effects on the regulation of Osmoregulated periplasmic glucans (OPGs)-induced c-di-GMP production and biofilm formation in Y. enterocolitica
Rcs and EnvZ/OmpR phosphorelays exert the opposite effects on the regulation of OPGs-induced cyclic dimeric guanosine monophosphate (c-diGMP) and biofilm production in Y. enterocolitica

Summary

Introduction

Yersinia enterocolitica is a common foodborne pathogen which causes a zoonotic disease called yersiniosis manifested in humans by acute gastroenteritis and sometimes more serious conditions such as pseudoappendicitis and even sepsis (Huovinen et al, 2010; Bari et al, 2011; Fabrega and Vila, 2012). Y. enterocolitica is widely distributed in the environment and can be found in soil, water, animals and various food products (Bari et al, 2011; Rahman et al, 2011), where constant changes in physicochemical conditions, including osmolarity, pH, temperature, light intensity, medium viscosity, and nutrient availability often threaten bacterial survival (Bottone, 1997; Brzostek et al, 2012) These challenges are met by rapid adaptation of the pathogen to varying growth conditions provided by two-component regulatory systems (TCSs), called phosphorelays, as they sense the extracellular signals and perform cascade phosphorylation in response, regulating the expression of genes related to flagellar synthesis, biofilm formation, and virulence (Clarke, 2010; Clarke and Voigt, 2011; Brzostek et al, 2012; Liu et al, 2017). The EnvZ/OmpR phosphorelay has been reported to be a central regulation system of several cellular responses in Y. enterocolitica (Brzostek et al, 2012)

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